Disease Index for the Rust Puccinia psidii on Apple in Hawai‘i

Robert C. Anderson1,2 and Janice Y. Uchida2 1U.S. Geological Survey, Pacific Island Ecosystems Research Center 2UH-CTAHR Department of and Environmental Protection Sciences

College of Tropical Agriculture and Human Resources

UNIVERSITY OF HAWAI‘I AT MÄNOA Introduction In 2005, Puccinia psidii, an invasive fungus causing rust in Brazil, was discovered on potted of ‘öhi‘a (Metrosideros polymorpha), on O‘ahu. This rust infects several members of the , including rose apple and paperbark, but thus far infections of the common guava have been rare. Urediniospores are the most common type of spores formed by this rust. These bright yellow spores are spherical with tiny spines, easily airborne, and have resulted in distribution of the disease to all major islands in Hawai‘i. Rose apple ( jambos) has been devastated in parts of the state exposed to extended periods of moist weather. The disease also occurs in dry areas, but is less severe. Personnel with the federal government, such as the U.S. Forest Service, U.S. Geological Survey, and APHIS, and state agencies, such as the Department of Land and Natural Resources and the Department of Agriculture, are concerned about the extent of the rust’s movement in Hawai‘i. Thus efforts to survey forests, surrounding plant communities, and commercial nurseries were deemed to be of high priority. Hikers and agency field workers can aid in this survey. To gather helpful data, observations of locations of the rust, the disease severity, and the environmental conditions are important. To help organize the disease survey, this disease index on rose apple, the most severely infected host, was prepared. Young tissues that are diseased will be covered with few to many spots (Category 3 or 4). Spores (urediniospores) are formed in groups called pustules on the leaf spot. Leaf spots that are old will have only a few urediniospores, and older spores become white, but the tiny spines remain. On older spots, pustules that are slightly more orange or brown contain two- celled teliospores that are longer and have no spines. Teliospores can occur in any category on older lesions or spots and can be formed along with urediniospores in the same pustule.

This is CTAHR Plant Disease publication PD-37, Feb. 2008. On the cover Rose apple tree infected with Puccinia psidii along Häna Highway, Maui, March 2007 (photo- graph by Forest and Kim Starr). Photo credits: Photos of Category 4 leaf and stem distortion and Category 5 branch tip dieback and severely diseased stand were taken by Forest and Kim Starr; all other photographs were taken by R. Anderson.

Published by the College of Tropical Agriculture and Human Resources (CTAHR) and issued in furtherance of Cooperative Extension work, Acts of May 8 and June 30, 1914, in cooperation with the U.S. Department of Agriculture. Andrew G. Hashimoto, Director/Dean, Cooperative Extension Service/CTAHR, University of Hawai‘i at Mänoa, Honolulu, Hawai‘i 96822. An equal opportunity/affirmative action institution providing programs and services to the people of Hawai‘i without regard to race, sex, age, religion, color, national origin, ancestry, disability, marital status, arrest and court record, sexual orientation, or status as a covered veteran. CTAHR publications can be found on the website www.ctahr.hawaii.edu/freepubs. 2 A series of disease indexes is being prepared to describe the Puccinia rust disease and to aid in monitoring it. In addition to this index on rose apple, others on ‘öhi‘a and other P. psidii hosts such as paperbark (Melaleuca quinquenervia) and are being prepared. Anyone helping with this survey is sincerely appreciated and should report findings to one of the researchers listed on the back cover. If you observe symptoms other than those described here, or if you have questions, please contact the authors.

Disease symptoms Rose apple is a highly susceptible host to Puccinia psidii rust in Hawai‘i and elsewhere. Rose apple leaves, stems, , and flowers can be affected, and the disease severity varies with the time of year. This plant is naturalized in the Hawaiian Islands in mesic to wet sites at elevations of 15Ð500 m (50Ð 1650 ft), primarily in valleys and occasionally in disturbed mesic forests. Symptom severity is based on the age of the plant tissue, the environmental moisture and temperature, and the amount of time since infection. Young leaf tissues are usually most heavily diseased by the rust and typically become blighted and deformed.

Wet weather symptoms Moisture is needed for infection, and disease severity increases during rainy or humid weather. Often, young tissues will be heavily infected with urediniospores (Category 4, page 8) during wet weather, while older leaves may have only a few lesions or spots (Category 1, page 5, or Category 2, page 6). When severely infected, leaves are blighted and deformed, and stems and leaves are often abundantly covered with yellow urediniospores. The urediniospores are the repeating stage of the rust, and they increase the epidemic by infecting new hosts or host tissue in the vicinity or miles away. Heavily infected leaves usually blacken and die, and after a month or so fall off, leaving only blackened stem tips (Category 5, page 9).

Dry weather symptoms On young leaf tissue during dry weather, instead of the whole leaf becoming 1 3 diseased, individual lesions approximately 3Ð5 mm ( ⁄8Ð ⁄16 inch) in diameter 3 form. Adjacent lesions sometimes coalesce to become 10 mm ( ⁄8 inch) or more in diameter. The lesions are reddish and have yellow urediniospores. As the leaves mature, the spots remain (Category 1 or 2), but fewer spores are formed. Six to eight weeks after the initial infection, spore formation is rare.

3 Making evaluations in the field

¥ For all sites, record the host plant, location, date, and disease category (as described below). A survey form is provided on page 11.

¥ For location, GPS coordinates are ideal. Lacking a GPS device, if you are on a trail, you can note which part you are on by estimating the distance traveled (first quarter of the trail, half way along, etc.), or you can note some land feature (near a certain stream, ridge, etc.); if near a highway, give its name and nearest milepost marker if available.

¥ Determine if the rust is present at a site by checking all sides of at least five trees; if no rust is found, the site’s record is zero (absence of the rust at a site is useful information). For tall trees, check the lower canopy and make a note of the tree size.

¥ Place specimens in separate bags and wipe hands with a moist tissue before handling a new plant. Avoid touching healthy plants if you have handled plants with heavy infection levels. Wiping hands is recommended after each sampling. Although movement of the pathogen is largely by the wind and rain splash, contact can also move spores.

¥ In the field, evaluators should rate a site or tree using the highest category for the rating. When a tree is severely infected and young stems are covered with spores, the disease is Category 4, even if the older leaves have only a few spots (Category 1 or 2). Note the category of the older leaves, buds, flowers, and , if present. When a tree has only old growth with dead branch tips, the disease is Category 5, but you should also make a note if there are other leaves in Category 1 to 3, and check for any other plant parts, such as flowers, that may be diseased.

4 Category 1 ¥ Ten spots or fewer per leaf, each spot about 1 3 2 mm ( ⁄16 inch) to more than 10 mm ( ⁄8 inch) in diameter. ¥ Leaves have few urediniospores and, if present, few teliospores. This category indicates that young leaves were infected when the inoculum level was very low, the environment was dry, or the leaf was mature enough to express some resistance. These leaves matured, developing only a few spots. Close-up of leaf spots and empty pustules

Abaxial Adaxial (leaf undersurface) (leaf upper surface) Abaxial

5 Category 2 ¥ More than 10 spots per leaf. ¥ Leaf spots may merge, causing formation of larger necrotic areas that are 25 mm (1 inch) or more long. ¥ Urediniospores are few, and teliospores may be present. ¥ Shot-holes, created by the loss of the diseased tissue, may also be present. As in Category 1, this level of spotting may reflect a low inoculum level, low environmental humidity, Close-up of leaf spot and or host resistance due to leaf maturity at the time empty pustules the leaves were infected.

Abaxial Abaxial Adaxial

6 Category 3 ¥ Occurs on young leaves. ¥ Less than 30 percent of the leaf area is covered with rust pustules. ¥ Leaves are not severely infected, and stem lesions are rare. ¥ Check for presence of teliospores. This generally represents infection of young tissue when the environment was Close-up of two clusters of pus- dry. tules (groups of urediniospores)

Adaxial, few spores Abaxial, many pustules and urediniospores

7 Category 4 ¥ Severe infection of young leaves and new growth, with as much as 80Ð100 percent of the leaf surface covered with lesions. ¥ Leaves may be deformed, curled, or distorted. ¥ Lesions present on stems. ¥ Urediniospores are produced in large numbers and frequently fall like powder onto the lower leaves. ¥ Check for presence of teliospores. During this epiphytotic (or plant epi- demic), heavy rust growth and pustule formation causes young tissues to Abaxial leaf Close-up of stem produce deformed new growth covered surface lesions and with yellow urediniospores. uredinia, or pustules

Deformed apical tip and red, deformed leaves Deformed leaves and stem

8 Category 5 ¥ Leaves become necrotic (blackened) and abscise (drop from the stem). ¥ Branch tips are severely diseased and bare of leaves (photo below, and p. 10). Following an epiphytotic on the young leaves, stems tips have no leaves and are brown or blackened. Dead branch tips are present in the upper canopy of the tree. Mature green leaves have Category 1 and 2 disease levels. New leaves produced on lower branches also become infected (Category 3 or 4).

Necrotic (dead) young leaves caused by severe infection (Category 4)

Close-up of branch tip dieback (new leaves circled)

9 Category 5 (continued) Other symptoms Pustules may be present on rose apple buds, flowers, and fruits.

Rose apple stand with severely dis- Infected inflorescence eased plants, Huelo, Maui

Infected bud, opening

For further information http://nt.ars-grin.gov/taxadescriptions/factsheets/ index.cfm?thisapp=Pucciniapsidii www.hear.org/species/puccinia_psidii For survey form Infected fruit www.ctahr.hawaii.edu/oc/forms/rustsurvey.pdf 10 Field survey for Puccinia psidii rust disease

Host observed: R rose apple R ‘Ŀhi‘a other ______Use a separate form for each host/observation.

Collector ______date __/__/__ phone/e-mail ______R sample taken; sample no. ______(Sample number might include your initials, the date, and a sequence number; e.g., RA 4/15/08–2. Please give this form to the researcher along with the sample.) Environment R nursery R natural location island ______location ______trail/road ______trail section/milepost ______elev. (est.) ______GPS ______0MUV.7:PUJS\KLM\Y[OLYKLZJYPW[PVUVM[OLZP[LPU[OLJVTTLU[ZÄLSK Description of plant R young RTH[\YL^P[OÅV^LYZHUKZLLKZR in decline, repeated loss of young leaves plant size ______For ‘Ŀhi‘a: R leaves pubescent (hairy) R leaves glabrous (smooth) ÅV^LYJVSVY!FFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFFF Rust occurrence leaf spots/rust spores R not observed R present disease index category: R 1 R 2 R 3 R 4 R 5 (check all that apply) ,_[LU[VMÄLSKL_HTPUH[PVU R 4 sides of host checked, at least 2–3 branches on each side examined; ______sides checked and branches examined; R only 1 side observed Disease present R mostly on young leaves R mature leaves R old leaves R all leaves Extent of rust infection in area: R 1 tree only R a few trees R many trees R all trees in the area have some infection Nearby infected host plants R rose apple R ‘Ŀhi‘a R paperbark R java plum R mountain apple R bush cherry R downy rose myrtle R Eugenia reinwardtiana others ______Other Metrosideros species present: R rugosa R macropus R waialealae R tremuloides M. polymorpha varieties present (specify) ______

Comments:

9LZLHYJOLYÄUKPUNZ! initials ______date ______R urediniospores R teliospores 11 Please submit rust survey results to these researchers:

O‘ahu Janice Y. Uchida. Dept. of Plant and Environmental Protection Sciences, College of Tropical Agriculture and Human Resources (CTAHR), University of Hawai‘i at Mänoa, St. John Hall 304, 3190 Maile Way, Honolulu, HI 96822; 808-956-2827; [email protected] Robert Anderson. Pacific Island Ecosystems Research Center, U.S. Geological Survey, 677 Ala Moana Blvd Ste 615, Honolulu, HI 96813; 808-587-7459; [email protected] Robert Hauff. Div. of Forestry and Wildlife, Hawai‘i Dept. of Land and Natural Resources, 1151 Punchbowl St Rm 325, Honolulu, HI 96813; 808-587-4174; [email protected]

Maui Norman Nagata. Cooperative Extension Service (CES), CTAHR, 310 Ka‘ahuamanu Ave, Bldg 214, Kahului, HI 96732; 808-244-3242 (ext. 230); [email protected]

Big Island Scot Nelson. CES, CTAHR, 875 Komohana St, Hilo, HI 96720 (mail only); 920 Stainback Hwy, Pana‘ewa (for visits and courier service); 808-981-8265; [email protected] J.B. Friday. CES, CTAHR, 875 Komohana St., Hilo, HI 96720 (mail only); 920 Stainback Hwy, Pana‘ewa (for visits and courier service); 808-981-8265; [email protected] Anne Marie LaRosa. Inst. for Pacific Islands Forestry, USDA Forest Service; 60 Nowelo St, Hilo, HI 96720; 808-933-8121 (ext. 115); [email protected]

Kaua‘i Jeri Ooka. Kaua‘i Agricultural Research Center, CTAHR, 7370-A Kuamo‘o Rd, Kapa‘a, HI 96746; 808-822-4984 (ext. 226 or 228); [email protected]

We greatly appreciate any findings of new hosts. If you find a plant not mentioned in this publication that may have the rust, please submit it to Janice Uchida, Robert Anderson, Robert Hauff, Scot Nelson, Norman Nagata, or Jeri Ooka. We will confirm the pathogen and report back to you.

College of Tropical Agriculture and Human Resources

UNIVERSITY OF HAWAI‘I AT MÄNOA